Torsional behavior of chromatin is modulated by rotational phasing of nucleosomes

Torsionally stressed DNA plays a critical role in genome organization and regulation. While the ef-fects of torsional stresses on naked DNA have been well studied, little is known about how these stresses propagate within chromatin and affect its organiza-tion. Here we investigate the torsional behavior of nucleosome arrays by means of Brownian dynam-ics simulations of a coarse-grained model of chro-matin. Our simulations reveal a strong dependence of the torsional response on the rotational phase an-gle Ψ 0 between adjacent nucleosomes. Extreme val-ues of Ψ 0 lead to asymmetric, bell-shaped extension-rotation profiles with sharp maxima shifted toward positive or negative rotations, depending on the sign of Ψ 0, and to fast, irregular propagation of DNA twist. In contrast, moderate Ψ 0 yield more symmetric pro-files with broad maxima and slow, uniform propa-gation of twist. The observed behavior is shown to arise from an interplay between nucleosomal transi-tions into states with crossed and open linker DNAs and global supercoiling of arrays into left- and right-handed coils, where Ψ 0 serves to modulate the en-ergy landscape of nucleosomal states. Our results also explain the torsional resilience of chromatin, reconcile differences between experimentally mea-sured extension-rotation profiles, and suggest a role of torsional stresses in regulating chromatin assem-bly and organization